Representation of Functional Category in the Monkey Prefrontal Cortex and Its Rule-Dependent Use for Behavioral Selection

Tsutsui, Ken; Hosokawa, Toru; Yamada, Munekazu; Iijima, Toshio

doi:10.1523/jneurosci.2063-15.2016

Cited by 14 publications

(14 citation statements)

References 59 publications

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“…Macaque monkeys are widely used in neurophysiological studies; thus, we can study neural mechanisms underlying the formation and usage of category in monkeys by using a group reversal task. We have recently recorded neuronal activity in the prefrontal cortex while the monkeys were performing the same task used in this study, and found that a subset of prefrontal neurons code category information 26 . It is expected that, by using the group reversal task, the neural mechanisms of category formation and utilization would be studied extensively, which may lead us to deeper understandings of higher cognitive functions.…”

Section: Discussionmentioning

confidence: 88%

Behavioral evidence for the use of functional categories during group reversal task performance in monkeys

Hosokawa

Honda

Yamada

et al. 2018

Sci Rep

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A functional category is a set of stimuli that are regarded as equivalent independently of their physical properties and elicit the same behavioral responses. Major psychological theories suggest the ability to form and utilize functional categories as a basis of higher cognition that markedly increases behavioral flexibility. Vaughan claimed the category use in pigeons on the basis of partition, a mathematical criterion for equivalence, however, there have been some criticisms that the evidence he showed was insufficient. In this study, by using a group reversal task, a procedure originally used by Vaughan, we aimed to gather further evidence to prove the category use in animals. Macaque monkeys, which served as subjects in our study, could efficiently perform the task not only with familiar stimulus sets as Vaughan demonstrated but also with novel sets, and furthermore the task performance was stable even when the number of stimuli in a set was increased, which we consider as further evidence for the category use in animals. In addition, by varying the timing of the reversal, we found that a category formation takes place soon after encountering new stimuli, i.e. in a few blocks of trial after a novel stimulus set was introduced.

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Section: Discussionmentioning

confidence: 88%

Behavioral evidence for the use of functional categories during group reversal task performance in monkeys

Hosokawa

Honda

Yamada

et al. 2018

Sci Rep

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“…Once a working rule has been generated, these neurons may exhibit top-down control to regions such as the inferior temporal cortex and the posterior parietal cortex (Freedman et al 2003;Antzoulatos and Miller 2016). Besides the lPFC, rule use and selective attention in category learning is evident across the PFC, including medial PFC, anterior cingulate cortex, and the ventromedial PFC (Grinband et al 2006;Seger et al 2015;Tsutsui et al 2016;Mack et al 2017;Bowman and Zeithamova 2018). Assuming that the rat PFC is homologous to the mPFC of primates, we hypothesize that rat selective attention mechanisms mediate RB task learning.…”

Section: Discussionmentioning

confidence: 96%

Selective attention in rat visual category learning

et al. 2019

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A prominent theory of category learning, COVIS, posits that new categories are learned with either a declarative or procedural system, depending on the task. The declarative system uses the prefrontal cortex (PFC) to learn rule-based (RB) category tasks in which there is one relevant sensory dimension that can be used to establish a rule for solving the task, whereas the procedural system uses corticostriatal circuits for information integration (II) tasks in which there are multiple relevant dimensions, precluding use of explicit rules. Previous studies have found faster learning of RB versus II tasks in humans and monkeys but not in pigeons. The absence of a learning rate difference in pigeons has been attributed to their lacking a PFC. A major gap in this comparative analysis, however, is the lack of data from a nonprimate mammalian species, such as rats, that have a PFC but a less differentiated PFC than primates. Here, we investigated RB and II category learning in rats. Similar to pigeons, RB and II tasks were learned at the same rate. After reaching a learning criterion, wider distributions of stimuli were presented to examine generalization. A second experiment found equivalent RB and II learning with wider category distributions. Computational modeling revealed that rats extract and selectively attend to category-relevant information but do not consistently use rules to solve the RB task. These findings suggest rats are on a continuum of PFC function between birds and primates, with selective attention but limited ability to utilize rules relative to primates.

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“…Frequency-dependent increases in their synchrony have been seen during shifts of attention (Buschman and Miller, 2007) and during visual working memory (Salazar et al, 2012), functions long associated with both regions. More recently, single-neuron studies indicate that both areas also make a major contribution to visual categorization (Antzoulatos and Miller, 2011; Cromer et al, 2010; Crowe et al, 2013; Freedman et al, 2001; Freedman and Assad, 2006; Goodwin et al, 2012; Rishel et al, 2013; Roy et al, 2010; Swaminathan and Freedman, 2012; Tsutsui et al, 2016). Individual neurons in both areas carve up different types of sensory information (i.e., motion, shape, location) according to learned category boundaries.…”

Section: Introductionmentioning

confidence: 99%

Synchronous beta rhythms of frontoparietal networks support only behaviorally relevant representations

Antzoulatos

Miller

2016

eLife

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Categorization has been associated with distributed networks of the primate brain, including the prefrontal cortex (PFC) and posterior parietal cortex (PPC). Although category-selective spiking in PFC and PPC has been established, the frequency-dependent dynamic interactions of frontoparietal networks are largely unexplored. We trained monkeys to perform a delayed-match-to-spatial-category task while recording spikes and local field potentials from the PFC and PPC with multiple electrodes. We found category-selective beta- and delta-band synchrony between and within the areas. However, in addition to the categories, delta synchrony and spiking activity also reflected irrelevant stimulus dimensions. By contrast, beta synchrony only conveyed information about the task-relevant categories. Further, category-selective PFC neurons were synchronized with PPC beta oscillations, while neurons that carried irrelevant information were not. These results suggest that long-range beta-band synchrony could act as a filter that only supports neural representations of the variables relevant to the task at hand.DOI: http://dx.doi.org/10.7554/eLife.17822.001

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Representation of Functional Category in the Monkey Prefrontal Cortex and Its Rule-Dependent Use for Behavioral Selection

Cited by 14 publications

References 59 publications

Behavioral evidence for the use of functional categories during group reversal task performance in monkeys

Behavioral evidence for the use of functional categories during group reversal task performance in monkeys

Selective attention in rat visual category learning

Synchronous beta rhythms of frontoparietal networks support only behaviorally relevant representations

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